Reviewing the effects of contamination on the biota of Brazilian coastal ecosystems: Scientific challenges for a developing country in a changing world.

Pollution is a major worldwide problem that is increasing with urban growth, mainly along coastal areas. Pollution is often worse, governance is poorer and managerial strategies to improve environmental quality are less advanced in developing than developed countries. Here, we present an overview of the current scientific knowledge of the impacts of contamination on the biota of coastal ecosystems of Brazil and evaluate the scientific challenges to provide baseline information for local managerial purposes. We compiled data from 323 peer-reviewed published papers from the extensive Brazilian coast. We critically evaluated the produced knowledge (target contaminants, sources, ecosystems, taxa, response variables) and the science behind it (rigour and setting) within its socioenvironmental context (land occupation, use of the coast, sanitation status, contamination history). Research was driven largely by environmental outcomes of industrial development with a focus on the single effects of metals on the biota. The current knowledge derives mainly from laboratory manipulative experiments or from correlative field studies of changes in the biota with varying levels of contamination. Of these, 70% had problems in their experimental design. Environmental impacts have mainly been assessed using standard indicators of populations, mostly in ecotoxicological studies. Benthic assemblages have mostly been studied using structural indicators in field studies. Future assessments of impacts should expand research to more taxonomic groups and ecosystem compartments, adding combined functional and structural responses. Furthermore, further investigations need to consider the interactive effects of contaminants and other environmental stressors. By doing so, researchers would deliver more robust and effective results to solve problems of pollution.

Ten new species of Phyllodoce Lamarck, 1818 (Phyllodocidae, Annelida) from Brazil.

Herein we provide a taxonomic revision of Phyllodoce species from Brazil, describing 10 new species in addition to two new records, Phyllodoce longipes Kinberg, 1866 and Phyllodoce cf. madeirensis Langerhans, 1880. Phyllodoce sp. A. and Phyllodoce sp. B. are probably new but the number and condition of available specimens do not provide adequate and reliable diagnostic features for a formal description. These species have been collected in diverse marine and estuarine environments from shallow estuarine bottoms to continental shelf and slope sediments and submarine canyons from off southern and southeastern Brazil. A key to the fourteen species of Phyllodoce occurring in Brazil is also given.

Seasonal variation of oxidative biomarkers in gills and digestive glands of the clam Anomalocardia flexuosa and the mangrove oyster Crassostrea rhizophorae.

We determined values of antioxidant biomarkers catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GPx), glutathione S-transferase (GST) and malondialdehyde (MDA) in two bivalve species from a subtropical system in Brazil. Differences in the biomarkers activities measured in digestive glands and gills sampled at two seasons and in sites with different levels of contamination were tested using univariate and multivariate analyses. Seasonality was the main factor accounting for overall variability. Significant SOD and GPx activities and increased levels of lipid peroxides were detected in summer, while CAT activity was higher in winter. However, biomarkers respond to complex environmental settings as indicated by the significant interaction between season and contamination level. We propose A. flexuosa as a candidate for monitoring studies with sampling occurring at a yearly timescale, and using C. rhizophorae is better suited for designs that include both seasons.

Euryhalinity of subtropical marine and estuarine polychaetes evaluated through carbonic anhydrase activity and cell volume regulation.

Polychaete worms are widespread and diverse in marine and estuarine habitats subject to varying salinity, in areas influenced by tides, demanding physiological adjustment for internal homeostasis. They are typically considered and reported to be osmoconformers, but they are not often studied for their osmoregulation. Here, three species of polychaete worms from distinct coastal habitats have been investigated: the spionid Scolelepis goodbody (intertidal in saline, exposed sandy beaches), the nereidid Laeonereis culveri (estuarine polyhaline), and the nephtyid Nephtys fluviatilis (estuarine oligohaline). The general objective here was to relate ecological aspects and physiology of the studied species. Constitutive whole body osmolality and carbonic anhydrase activity (CAA, relevant for osmoregulation, acid-base balance and respiration) have been assayed. In addition, cell volume regulatory capacity (from whole body cell dissociation) was challenged under hypoosmotic and hyperosmotic shocks (50% intensity), with respect to isosmotic control. S. googdbody and L. culveri, the two species from most saline environments (marine/estuarine), showed higher CAA than N. fluviatilis, which, in turn, displayed a hyperosmotic gradient to water of salinity 15. Cells from S. goodbody and L. culveri showed regulatory volume decrease upon swelling, with S. goodbody showing the largest volume increase. As in other more studied marine invertebrate groups, polychaetes also show variability in their osmoregulatory physiology, related to distinct saline challenges faced in their coastal habitats.

Metataxonomic and metagenomic analysis of mangrove microbiomes reveals community patterns driven by salinity and pH gradients in Paranaguá Bay, Brazil.

While environmental drivers regulate the structure of mangrove microbial communities, their exact nature and the extent of their influence require further elucidation. By means of 16S rRNA gene-based sequencing, we determined the microbial taxonomic profiles of mangroves in the subtropical Paranaguá Bay, Brazil, considering as potential drivers: salinity, as represented by two sectors in the extremes of a salinity gradient (<5 PSU and >30 PSU); proximity to/absence of the prevailing plants, Avicennia schaueriana, Laguncularia racemosa, Rhizophora mangle, and Spartina alterniflora; and the chemical composition of the sediments. Salinity levels within the estuary had the strongest influence on microbial structure, and pH was important to separate two communities within the high salinity environment. About one fourth of the total variation in community structure resulted from covariation of salinity and the overall chemical composition, which might indicate that the chemical profile was also related to salinity. The most prevalent bacterial phyla associated with the mangrove soils analyzed included Proteobacteria, Actinobacteria, Chloroflexi, Bacteroidetes, Acidobacteria, and Cyanobacteria. Taxonomic and functional comparisons of our results for whole-genome sequencing with available data from other biomes showed that the studied microbiomes cluster first according to biome type, then to matrix type and salinity status. Metabolic functions were more conserved than organisms within mangroves and across all biomes, indicating that core functions are preserved in any of the given conditions regardless of the specific organisms harboring them.

Petroleum biomarkers as tracers of low-level chronic oil contamination of coastal environments: A systematic approach in a subtropical mangrove.

Petroleum biomarkers (hopanes, terpanes and steranes) are frequently assessed in estuarine sediments as tracers of oil input. In order to compare distinct patterns of hydrocarbon accumulation in mudflats, salt marsh and mangrove, sediments from two transects (control and impacted areas) were sampled in Paranaguá Bay, SW Atlantic. Concentrations of n-alkanes, polycyclic aromatic hydrocarbons (PAHs) and petroleum biomarkers (hopanes, terpanes and steranes) were determined, as well as bulk parameters (TOC, grain size and δ13C). N-alkanes concentrations were similar between control and impacted sites (respectively, 3.03 ±â€¯1.20 µg g-1 and 4.11 ±â€¯3.02 µg g-1) and reflected a high biogenic input. Conversely, PAHs and petroleum biomarker concentrations were three to six times higher in impacted site than the control site (respectively, 60.4 ±â€¯23.3 ng g-1 and 22.0 ±â€¯25.0 ng g-1 for PAHs and 197.7 ±â€¯51.8 ng g-1 and 40.2 ±â€¯32. ng g-1 for hopanes). Despite these differences, concentrations were lower than those reported for highly impacted areas worldwide. Diagnostic ratios and hydrocarbon parameters (e.g. total PAHs and total petroleum biomarkers) helped to distinguish human impact in the ecological zones, suggesting different sources and/or levels of weathering, confirmed by ANOVA tests. TOC played a fundamental role to the concentration of hydrocarbons, showing similar distributions along the transects. Petroleum biomarkers could clearly indicate the preferential sites of deposition and assign different levels of anthropic contamination by hydrocarbons, thus providing clear information about the chronic petroleum pollution in coastal sediments.

Four new species of Paranaitis Southern, 1914 (Phyllodocidae, Annelida) from southern and southeastern Brazil.

Four new species of Paranaitis are described from estuarine and continental shelf bottoms from southern and southeastern Brazil: Paranaitis chitinosa sp. nov., P. cirriformata sp. nov., P. assimetrica sp. nov., and P. cordiformata sp. nov. Paranaitis chitinosa sp. nov. is diagnosed by a proboscis with rows of conical and chitinous papillae alternating with dorsal chitinous bars, and the distal extremity covered with micropapillae, and dorsal cirri rounded and asymmetrical. Paranaitis cirriformata sp. nov. is similar to P. speciosa (Webster, 1879), previously recorded from Brazil, but differs by the presence of long and slender anal cirri. Paranaitis assimetrica sp. nov. differs from P. cordiformata sp. nov. by the presence of supra-acicular lobes that are considerably longer than the subacicular ones, and oval dorsal cirri. Paranaitis cordiformata sp. nov. has cordiform dorsal cirri and symmetrical supra- and sub-acicular lobes.

Strategies for tube construction in Owenia caissara (Oweniidae, Annelida) from southern Brazil.

In this paper, we have experimentally assessed tube-building strategies of Owenia caissaraSilva & Lana, 2017, including the particle size preferences. After acclimation, individual tubes were broken by their mid-region, and placed in experimental aquaria with four types of homogeneous substrates (from silt-clay to coarse sand) and four types of mixed substrates. Animals completely removed from their tubes were unable to build new tubes. Adults in broken tubes were able to use a wide range of particles, from fine to coarse sand, but not silt-clay. Owenia caissara showed a clear preference for coarse sediment particles. In extreme conditions, individuals were able to rebuild their tubes using only filamentous debris. Owenia caissara may display higher selection ability and preference for larger particles when growing, although adults can also adapt to bottoms with predominantly smaller particles such as fine sand.

Testing biomarker feasibility: a case study of Laeonereis culveri (Nereididae, Annelida) exposed to sewage contamination in a subtropical estuary.

The feasibility of biomarkers to accurately detect pollution in estuaries and coastal areas appears to be overestimated in the scientific literature, and is likely stemming from a bias towards publishing only positive results. Herein, we test the applicability of antioxidant capacity and lipid peroxidation to detect potential in situ sewage impacts on a subtropical estuary. We experimentally assessed variation in malondialdehyde (MDA, an indicator of lipid peroxidation) and total antioxidant capacity against peroxyl radicals (ACAP) through transplantations of the worm Laeonereis culveri from control to sewage-polluted areas. Variations in biomarkers were more related to natural environmental variability and small-scale heterogeneity among areas than to experimental exposure to sewage. Use of oxidative stress biomarkers is promising but further experimental work under real-life conditions is necessary to further validate and establish their accuracy and feasibility for practical purposes.

Effects of an in situ diesel oil spill on oxidative stress in the clam Anomalocardia flexuosa.

Intensive exploitation and transport of oil and derivatives are increasing the risk of coastal contamination by either dramatic disasters or diffuse sources. Tools for monitoring diffuse contamination, such as diesel oil that leaks from marine vessels are much needed. We experimentally tested the efficiency of antioxidant biomarkers as indicators of chronic exposure to diesel oil in a mudflat from the subtropical Bay of Paranaguá, in southern Brazil. We examined the effects of three successive diesel oil spills, with two weeks of recovery time between exposures, on the edible clam Anomalocardia flexuosa. Previous studies have highlighted its potential as a bioindicator species for diesel oil contamination in subtropical and tropical ecosystems. Endpoints measured in gill and digestive gland homogenates included the activity of antioxidant enzymes SOD, GPx, GST and levels of lipid peroxides. PAHs concentration in sediments and soft tissue were also quantified. GST and SOD were the most responsive biomarkers to the exposure. There were significant but non-cumulative departures from control levels in organisms from treated samples, which were, in all cases, more common 48 h after each experimental spill. Biomarker responses were more evident in the digestive gland than in gills. This work validated the short-term responsiveness of biomarkers as measures of repeated pulsed in situ exposure to low concentrations of diesel oil. For their routine implementation into monitoring programs for tropical estuaries our general recommendations are 1) to include several reference sites, 2) to analyze biomarker data using a logarithmic-scale and 3) to interpret deviations from "normal" activity as multiplicative interval differences.

Owenia caissara sp. n. (Annelida, Oweniidae) from Southern Brazil: addressing an identity crisis

We re-assess the taxonomic status of Owenia Delle Chiaje, 1841 from Southern Brazil based on estuarine specimens from Paranaguá Bay (Paraná) and Babitonga Bay (Santa Catarina), and literature records. Owenia caissara sp. n. is diagnosed by a branchial crown with five pairs of tentacles, branched close to the base of the crown, rectilinear collar with a pronounced lateral slit, two ventrolateral ocelli partially covered by the collar, up to 23 hooks on a single row in the first abdominal segment, regularly curved nuchal shape, regularly moderate teeth curvature, and long and thin scales with oval transition. The description of Owenia caissara sp. n. reinforces the idea that Owenia fusiformis sensu lato is a complex of closely related species that can be distinguished on the basis of both macro- and micro- morphological traits.(AU)

Owenia caissara sp. n. (Annelida, Oweniidae) from Southern Brazil: addressing an identity crisis

We re-assess the taxonomic status of Owenia Delle Chiaje, 1841 from Southern Brazil based on estuarine specimens from Paranaguá Bay (Paraná) and Babitonga Bay (Santa Catarina), and literature records. Owenia caissara sp. n. is diagnosed by a branchial crown with five pairs of tentacles, branched close to the base of the crown, rectilinear collar with a pronounced lateral slit, two ventrolateral ocelli partially covered by the collar, up to 23 hooks on a single row in the first abdominal segment, regularly curved nuchal shape, regularly moderate teeth curvature, and long and thin scales with oval transition. The description of Owenia caissara sp. n. reinforces the idea that Owenia fusiformis sensu lato is a complex of closely related species that can be distinguished on the basis of both macro- and micro- morphological traits.

Sewage input reduces the consumption of Rhizophora mangle propagules by crabs in a subtropical mangrove system.

Mangrove forests are highly productive and play a major role in global carbon cycling. Their carbon accumulation can be influenced through the consumption of nutrient-poor leaves and propagules by herbivore crabs. Anthropogenic nutrient input from sewage contamination is widespread in these often naturally nutrient-limited ecosystems. We hypothesised that sewage-mediated nutrient input to mangrove stands of Paranaguá Bay (southern Brazil), would alter the nutrient sources available for crabs, e.g. through microphytobenthos increase, and that this would reflect in their feeding behaviour. We predicted that propagules of Rhizophora mangle in contaminated stands would experience lower grazing pressure from their two main local consumers (Ucides cordatus and Goniopsis cruentata). We compared herbivory rates on R. mangle propagules in sewage contaminated and uncontaminated mangrove stands. We found that herbivory rates were significantly lower in contaminated than uncontaminated forests, but this pattern could not be clearly attributed to increased nutrient availability.

Baseline levels of oxidative stress biomarkers in species from a subtropical estuarine system (Paranaguá Bay, southern Brazil).

Offshore petroleum exploration has increased the risks of oil spills in coastal tropical and subtropical habitats. Monitoring tools are needed to assess and protect environmental health. We determined baseline values of antioxidant biomarkers (CAT, SOD, GPx, GST, MDA) for five ecologically relevant species in a subtropical system in southern Brazil. Regional baseline levels are compared with literature data as a basis to eventually test their efficacy as post-spill monitoring tools. Differences in the antioxidant response among species, contamination, and seasons were tested using univariate and multivariate analyses. The bivalves Anomalocardia flexuosa and Crassostrea rhizophorae and the catfish Genidens genidens emerge as suitable sentinel species. Seasonality is the main factor accounting for biomarkers variability, and not background contamination level. However, interactions between season and contamination level are also significant, indicating that biomarkers respond to complex environmental settings, a fact that needs to be fully understood for designing proper monitoring programs.

Antioxidant responses in estuarine invertebrates exposed to repeated oil spills: Effects of frequency and dosage in a field manipulative experiment.

We have experimentally investigated the effects of repeated diesel spills on the bivalve Anomalocardia brasiliana, the gastropod Neritina virginea and the polychaete Laeonereis culveri, by monitoring the responses of oxidative stress biomarkers in a subtropical estuary. Three frequencies of exposure events were compared against two dosages of oil in a factorial experiment with asymmetrical controls. Hypotheses were tested to distinguish between (i) the overall effect of oil spills, (ii) the effect of diesel dosage via different exposure regimes, and (iii) the effect of time since last spill. Antioxidant defense responses and oxidative damage in the bivalve A. brasiliana and the polychaete L. culveri were overall significantly affected by frequent oil spills compared to undisturbed controls. The main effects of diesel spills on both species were the induction of SOD and GST activities, a significant increase in LPO levels and a decrease in GSH concentration. N. virginea was particularly tolerant to oil exposure, with the exception of a significant GSH depletion. Overall, enzymatic activities and oxidative damage in A. brasiliana and L. culveri were induced by frequent low-dosage spills compared to infrequent high-dosage spills, although the opposite pattern was observed for N. virginea antioxidant responses. Antioxidant responses in A. brasiliana and L. culveri were not affected by timing of exposure events. However, our results revealed that N. virginea might have a delayed response to acute high-dosage exposure. Experimental in situ simulations of oil exposure events with varying frequencies and intensities provide a useful tool for detecting and quantifying environmental impacts. In general, antioxidant biomarkers were induced by frequent low-dosage exposures compared to infrequent high-dosage ones. The bivalve A. brasiliana and the polychaete L. culveri are more suitable sentinels due to their greater responsiveness to oil and also to their wider geographical distribution.

Are intertidal soft sediment assemblages affected by repeated oil spill events? A field-based experimental approach.

This study investigates the impact of repeated diesel spills on the structure of intertidal macrofaunal assemblages of a subtropical estuary. Three frequencies of exposure events were compared against two dosages of oil in a factorial experiment with asymmetrical controls. Hypotheses were tested to distinguish between (i) the overall effect of oil spills, (ii) the effect of diesel dosage via different exposure regimes, and (iii) the effect of time since last spill. Repeated oil spills dramatically altered the overall structure of assemblages and reduced the total density of macrofauna and densities of dominant taxa. Increasing the frequency of oil spills negatively affected macrofauna. In general, frequent low-dosage oil spills were more deleterious than infrequent high-dosage ones. However, increases in densities of some taxa, mainly the gastropod Heleobia australis, were observed in response to infrequent spills. Our results highlight the importance of repeated exposure events in determining the extent of oil impacts.

Dissecting the distribution of brittle stars along a sewage pollution gradient indicated by organic markers.

We have assessed variation in brittle star distribution patterns along a contamination gradient identified by fecal steroids and aliphatic hydrocarbons in Paranaguá Bay, southern Brazil. A hierarchical design using multiple spatial scales (centimeters-kilometers) was applied. Generalized linear mixed models (GLMMs) were used to investigate the spatial and temporal variability of brittle stars. Main principal components from the contamination and environmental matrices were used to investigate the best explanatory dataset. The abundance of brittle stars was significantly lower in sites with high concentrations of fecal steroids and aliphatic hydrocarbons. The best model fitting always included components from the contamination gradients, which precludes a purely environmental driving of brittle star abundance. Variability in spatial scales lower than kilometers was probably driven by sediment characteristics. We highlighted the importance of a robust multi-scale sampling design for a better biological indication of coastal contamination.

Description of three new species of Eumida Malmgren, 1865 (Phyllodocidae, Annelida) from Southern and Southeastern Brazil.

We describe three new species of Eumida from shallow estuarine and shelf bottoms from south and southeastern Brazil as part of a regional survey of the family Phyllodocidae. Previous regional records of Eumida sanguinea (Örsted, 1843) are herein referred to Eumida dracodermica sp. nov. The two species differ in the size of the prostomium, the distribution of micropapillae on the proboscis, and the shape of the dorsal cirri. Eumida macrophthalma sp. nov. has much larger eyes than the other two species described herein. The dorsal cirri on anterior median segments are rounded and on median and posterior segments they are asymmetrical and cordiform, longer than the dorsal cirri in Eumida dracodermica sp. nov. The lanceolate median dorsal cirri in Eumida delicata sp. nov. are only shared with E. ockelmanni Eibye-Jacobsen, 1987. It is also possible to diagnose the three species by their dorsal whitish pigmentation patterns on the first segments of living or well conserved animals.